Abstract

Attention gates the processing of stimuli relatively early in visual cortex. Yet, existing data suggest that emotional stimuli activate brain regions automatically, largely immune from attentional control. To resolve this puzzle, we used functional magnetic resonance imaging to first measure activation in regions that responded differentially to faces with emotional expressions (fearful and happy) compared with neutral faces. We then measured the modulation of these responses by attention, using a competing task with a high attentional load. Contrary to the prevailing view, all brain regions responding differentially to emotional faces, including the amygdala, did so only when sufficient attentional resources were available to process the faces. Thus, the processing of facial expression appears to be under top-down control.

Experimental paradigm. While subjects fixated the faces, they indicated in alternating blocks of trials either whether the face was male or female (attended trials) or whether the bars were or were not of similar orientations (unattended trials). The dashed lines indicate the display regions attended on alternating blocks (not shown on actual displays). Stimuli are not drawn to scale.

Coupling of activity between the amygdala and other brain regions. (A) Increases in the coupling between amygdala and visual cortical activity (V1/V2 and fusiform gyrus; see arrows) on attended compared with unattended trials (see Materials andMethods). (B) Contrast of fearful and neutral faces during attended trials, demonstrating a significant effect of valence in the fusiform gyrus. A threshold of P < 0.00001 (uncorrected) was used for both A and B (which show the y = −52 plane). L, left; R, right.